review
review
Functional elements residing within satellite DNAs
Durdica Ugarkovic
Ruder Boskovic Institute, Zagreb, Croatia
Satellite DNAs represent a fast-evolving portion of the eukaryotic
genome whose evolution is proposed to be driven by the stochastic
process of molecular drive. Recent results indicate that satellite
DNAs are subject to certain structural constraints, which are
probably related to their interaction with proteins involved in the
establishment of specific chromatin structures. The evolutionary
persistence and high sequence conservation of some satellites, as
well as the presence of stage- or tissue-specific, differentially
expressed transcripts in several species, are consistent with the
hypothesis that satellite DNA could have a regulatory role in
eukaryotic organisms. Although the role of most transcripts is not
known, some act as precursors of small interfering RNAs, which
are now recognized as having an important role in chromatin modulation and the control of gene expression. Furthermore, some
transcripts are involved in the cellular response to stress.
Keywords: CENP-B box; gene regulation; heterochromatin;
noncoding RNA; repetitive DNA
EMBO reports (2005) 6, 1035–1039. doi:10.1038/sj.embor.7400558
Introduction
Satellite DNAs are tandemly repeated sequences that are present as
long uninterrupted arrays in genetically silent heterochromatic
regions (Charlesworth et al, 1994). Basic repeat units of satellite
DNAs usually have distinct complex sequences, such as the 171-bplong monomer of the human α-satellite, which represents a main
structural element of centromeric and pericentromeric regions
(Schueler et al, 2001). The most abundant mouse pericentromeric
γ−satellite also belongs to this group as it is composed of 234-bp
monomers of specific sequence (Rudert et al, 1995). However, other
satellites are composed of short simple repeats, such as human satellite III with a 5 bp-long monomer, as well as many of the Drosophila
satellites (Borstnik et al, 1994). Several different satellite DNAs are
usually present in a species and are subject to the influence of gene
conversion and unequal crossing over. These recombinational
mechanisms are responsible for the rapid horizontal spread of mutations among monomers in a genome. The mutations are subsequently fixed in reproductive populations through the stochastic process
of molecular drive (Dover, 1986). Copy number change and loss of
the satellite DNAs from the genome are also the result of unequal
Department of Molecular Biology, Ruder Boskovic Institute, Bijenicka 54, PO Box 180,
HR-10002 Zagreb, Croatia
Tel: +385 1 456 1083; Fax: +385 1 456 1177;
E-mail: [email protected]
Submitted 30 June 2005; accepted 20 September 2005
©2005 EUROPEAN MOLECULAR BIOLOGY ORGANIZATION
crossing over. The outcome of the recombinational mechanisms and
molecular drive is a high turnover of this part of the eukaryotic
genome. Therefore, satellite DNAs show significant rearrangements
and sequence divergence as well as changes in copy number, even
between closely related species (Ugarkovic & Plohl, 2002).
Despite their structural divergence and general lack of sequence
conservation across species, satellite DNAs are the main constituents of heterochromatin and act as a centromere-building element. They associate strongly with several proteins that form unique
centromeric heterochromatin (Henikoff & Dalal, 2005). Satellite
DNAs are not, however, a prerequisite for centromere establishment
and are instead proposed to drive the adaptive evolution of specific
centromeric histones (Cooper & Henikoff, 2004). In addition, transcripts of satellite DNAs in the form of small interfering RNAs
(siRNA) participate in the epigenetic process of chromatin remodulation and heterochromatin formation (Volpe et al, 2002; Verdel
et al, 2004). Recent data indicate that the evolution of satellite DNA
sequences is not only driven by molecular drive, but also influenced
by selective constraints (Hall et al, 2003; Mravinac et al, 2005). This
conclusion is based on the extreme sequence preservation and wide
evolutionary distribution of some satellite DNAs, as well as on the
conservation of particular structural motifs. Selective constraints on
satellite sequence are probably related to their interaction with specific proteins necessary for heterochromatin formation and to their
role in controlling gene expression. This review summarizes recent
studies on the presence of different structural elements of functional
importance found in diverse sequences of satellite DNA. In particular, the transcription of satellite DNA, which seems to be a general phenomenon, and the processing of transcripts into different
functional RNA molecules are discussed.
Common sequence motifs and structural features
Selection was first thought to influence satellite DNA sequences
after the observation of constant and variable regions in
Arabidopsis thaliana and human α-satellite DNA (Romanova et al,
1996; Heslop-Harrison et al, 1999). The significant difference in
mutation rate of distinct nucleotide positions is also characteristic
of human satellite III pentameric repeats (Borstnik et al, 1994). By
comparing more than 1,000 monomers, an analysis of the variability of A. thaliana satellite DNA and those from the insect genus
Tribolium has been performed. This clearly shows that the rate of
evolution is not uniform along the sequence (Hall et al, 2003;
Mravinac et al, 2004). Such a non-random pattern of variability
indicates possible functional constraints on satellite DNA sequence
that may be related to specific protein-binding sites.
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The most characterized satellite DNA-binding protein is
human centromere protein B (CENP-B), which binds to a 17-bp
motif in human α-satellite DNA known as the CENP-B box
(Masumoto et al, 1989). Proteins homologous to CENP-B have
been found in many eukaryotes, including the fission yeast
Schizosaccharomyces pombe, and motifs that are 60%–70% similar to the CENP-B box have been detected in diverse centromeric
repeats of mammals and insects (Kipling & Warburton, 1997;
Mravinac et al, 2004). Although only 23% of repeats in human
α-satellite DNA have a functional CENP-B box, it seems to be
essential for the assembly of centromere-specific chromatin (Fig
1; Ohzeki et al, 2002; Basu et al, 2005). Analysis of long higherorder α-satellite arrays revealed that CENP-B binding sites are
located in alternating repeat monomers (Ikeno et al, 1994). This
supports the model that only a subset of α-satellite monomers
binds CENP-B, which results in protein phasing and higher-order
chromatin structure (Yoda et al, 1998). In addition to the CENP-B
box, other relatively conserved oligonucleotide motifs have been
identified in different satellites. In avian centromeric satellites,
short oligonucleotide tracts are conserved in sequence and position whereas the rest of the sequence is highly divergent (Madsen
et al, 1994). Clustering of A or T and regular phasing of tracts of
three or more A + T combined with the presence of dyad structures has been reported for many different satellite DNAs
(Martinez-Balbas et al, 1990; Ugarkovic et al, 1996). Periodic distribution of AT tracts usually leads to curvature of the DNA helix
axis, which is characteristic of approximately 50% of satellite
DNAs (Fitzgerald et al, 1994). As a result of this curvature, a
superhelical tertiary structure is formed that is thought to be
important for the tight packing of DNA and proteins in heterochromatin (Fig 1; Ugarkovic et al, 1992; Fitzgerald et al, 1994).
Besides these conserved motifs, other more variable regions in
satellite DNAs may also be functionally important owing to their
interaction with rapidly evolving proteins. An example is the centromere-specific histone, CENH3, which replaces histone H3 in
centromeric nucleosomes and is required for proper chromosome
distribution during cell division (Henikoff & Dalal, 2005). Unlike
the highly conserved histone H3, CENH3 is divergent and subject
to the influence of positive selection, which particularly affects the
sites that potentially interact with satellite DNA (Cooper &
Henikoff, 2004). This suggests that variable regions are potential
drivers of CENH3 adaptive evolution and that they have a role in
the evolution of the centromere.
Ultra-conserved satellite sequences
Although, in general, satellite DNAs belong to the fast-evolving
portion of the eukaryotic genome, some are preserved for long
evolutionary periods and have a highly conserved monomer
sequence. Extreme sequence conservation of two satellite DNAs
that represent main pericentromeric repeats in the coleopteran
insect species Palorus ratzeburgii and Palorus subdepressus has
been reported (Mravinac et al, 2002, 2005). These satellites are
present in many coleopteran species at a low copy number and
their sequences have remained unchanged for 60 million years.
This remarkable antiquity and sequence conservation are also
characteristic of human α-satellite DNA, which has been detected
as a rare, highly conserved repeat in evolutionarily distant species
such as chicken and zebrafish (Li & Kirby, 2003). This complete
sequence conservation and the wide evolutionary distribution
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Functional elements in satellite DNAs
D. Ugarkovic
of some satellite sequences have led to the assumption that in
addition to participating in centromere formation, they might also
act as cis-regulatory elements of gene expression, as is observed
for some highly conserved, mammalian non-coding elements
(Frazer et al, 2004).
Satellite DNA transcripts
Transcripts of satellite DNAs have been reported in several organisms including vertebrates, invertebrates and plants. In most
species, satellite DNAs are temporally transcribed at particular
developmental stages or are differentially expressed in some cell
types, tissues or organs. Transcription has been detected during
embryogenesis in the newts Triturus cristatus carnifex (Varley et al,
1980) and Notophthalmus viridescens (Diaz et al, 1981).
Transcripts of an α-like satellite repeat detected during early
embryogenesis in chick and zebrafish were limited to the cardiac
neural crest, the head and the heart (Li & Kirby, 2003). Two types of
transcript were identified; one that corresponds to α-repeat RNA
and another group of mRNAs that contain an α-like satellite
sequence in the 5’ and 3’ untranslated regions. Mouse γ-satellite
DNA is differentially expressed during development of the central
nervous system, as well as in the adult liver and testis (Rudert et al,
1995). Transcripts have also been detected in hymenopteran insect
species (Rouleux-Bonnin et al, 1996), as well as on Y-chromosome
loops in primary spermatocyte nuclei of Drosophila melanogaster
(Bonaccorsi et al, 1990) and Drosophila hydei (Trapitz et al, 1988).
Most transcripts are present as polyadenylated RNA in the cytoplasm but some are found exclusively in the nucleus, such as those
associated with the Y chromosome of D. melanogaster and D. hydei
(Trapitz et al, 1988; Bonaccorsi et al, 1990). Transcripts are usually
heterogeneous in size and are in some cases strand-specific, as in
the mouse (Rudert et al, 1995), or transcription proceeds from both
DNA strands, as in Hymenoptera (Rouleux-Bonnin et al, 1996). The
developmental, stage- and tissue-specific expression of satellite
DNAs in several species suggest that they have a regulatory role,
although for most transcripts this role is still elusive and hypothetical. Taking into account the extreme sequence diversity of satellite
DNAs and their transcripts, several sequence-specific regulatory signals might reside within them. Targets of these signals could be other
RNAs, DNA or proteins. Regulatory interactions may also involve
secondary or tertiary structures of RNA and RNA-mediated catalysis.
Recently, it has been shown that heat shock induces the transcription of a subset of satellite III, which is located within pericentromeric heterochromatic regions of specific human chromosomes
( Jolly et al, 2004; Rizzi et al, 2004). Long, single-stranded
polyadenylated transcripts of satellite III are involved directly in the
recruitment of splicing factors to nuclear stress granules (Metz et al,
2004; Chiodi et al, 2004). It has been proposed that sequestration of
splicing factors within the granules through their association with
nuclear satellite III transcripts could regulate splicing function
during stress (Fig 1; Valgardsdottir et al, 2005). The satellite DNA
transcripts from salamanders (Epstein & Gall, 1987), schistosomes
(Ferbeyre et al, 1998) and crickets (Rojas et al, 2000) are expressed
as long multimeric precursor RNAs that have the ability to adopt
hammerhead-like secondary structures and can function as
ribozymes with self-cleavage activity. The products of self-cleavage
are satellite monomers that can act as ribozymes either in cis or
in trans (Fig 1). However, the physiological role of these ribozymes
is unknown.
©2005 EUROPEAN MOLECULAR BIOLOGY ORGANIZATION
review
Functional elements in satellite DNAs
D. Ugarkovic
AT
CENP-B box
AT
DNA curvature
Promoter
AT
AT
Transcription
Transcription
dsRNA
Chromatin
proteins
binding
Heterochromatin
formation
ssRNA
Splicing
factors
binding
Processing
Histone
methylation
siRNA
AT
Targeting
mRNA
Gene
regulation
Selfsplicing
Splicing regulation
during stress
Ribozymes
Fig 1 | Schematic representation of a satellite monomer and the processes in which satellite DNAs are involved. Common functional elements such as periodically
distributed AT tracts, centromere protein B (CENP-B) box and a promoter are indicated. A superhelical structure induced by DNA curvature, together with
chromatin proteins such as CENP-B, could contribute to heterochromatin formation. Transcription of satellite DNAs proceeds either in the form of doublestranded RNA (dsRNA) or single-stranded RNA (ssRNA). dsRNA is processed into small interfering RNAs (siRNAs) that participate in heterochromatin
formation and control expression of sequences tagged with complementary repeats. Single-stranded transcripts with hammerhead-like secondary structure have
self-cleavage activity and function as ribozymes. Some ssRNAs, such as human satellite III stress-induced transcripts, specifically recruit splicing factors to nuclear
stress granules and regulate splicing.
Promoters and transcription-factor binding sites
The characteristic sequence structure of some satellite DNAs is
based on simple repeats, which led to the proposal that they are
transcribed by read-through from upstream genes or transposable
element promoters (Diaz et al, 1981). However, potential regulatory
elements for RNA polymerase (pol) II and RNA pol III have been predicted in some satellite sequences (Renault et al, 1999). In schistosome satellite DNA, which encodes an active ribozyme, a functional
RNA pol III promoter is present (Ferbeyre et al, 1998). The sequence
of satellite 2 found in the newts Notophthalmus viridescens and
Triturus vulgaris meridionalis contains a functional analogue of the
vertebrate small nuclear RNA (snRNA) promoter that is responsible
for RNA pol II transcription (Coats et al, 1994). Human satellite III,
which is specifically expressed under stress, has a binding motif for
the heat-shock transcription factor 1 that drives RNA pol II transcription (Metz et al, 2004). Transcription factor YY1 associates with
γ−satellite DNA, which is located pericentromerically on all murine
chromosomes (Shestakova et al, 2004). YY1 belongs to the
Polycomb group of proteins that are involved in the repression of
homeotic genes, and its interaction with heterochromatin suggests a
link between these two silencing states.
Short interfering RNAs cognate to satellite DNAs
Recently, it has been shown that transcripts derived from tandemly
repeated centromeric DNA of the fission yeast S. pombe exist in the
form of small 20–25 bp-long RNAs that are involved in RNA interference (RNAi)-mediated heterochromatin assembly (Fig 1; Volpe
et al, 2002). This chromatin-silencing mechanism is initiated by
long double-stranded RNA (dsRNA) that arises from bidirectional
transcription of repeated DNA and is further processed by the
RNase III-like ribonuclease Dicer into siRNAs. siRNAs are then
©2005 EUROPEAN MOLECULAR BIOLOGY ORGANIZATION
loaded into the RNA-induced transcriptional silencing complex
(RITS) through their association with the Argonaute protein (Verdel
et al, 2004). RITS also interacts with the RNA-directed RNA polymerase complex (RDRC), which is required for the production of
secondary dsRNA and amplification of the silencing signal
(Motamedi et al, 2004). Both RITS and RDRC associate with the
nascent noncoding centromeric RNA transcript and binding to RITS
is probably achieved through the base-pairing of siRNA molecules
with nascent RNA and by direct contact with the RNA pol II elongation complex (Schramke et al, 2005; Kato et al, 2005). In addition to
siRNAs, the association of RITS with chromatin also requires a histone methyltransferase. Histone H3 methylation at lysine 9 (Lys 9) is
essential for the recruitment of the chromodomain protein Swi6, a
homologue of mammalian heterochromatin protein 1 (HP1). This
represents an initial step in the formation of heterochromatin.
Methylation of H3-Lys 9 also creates binding sites for RITS and
therefore enables further recruitment of heterochromatin assembly
factors (Noma et al, 2004). These studies show that the low level of
expression of satellite DNA is necessary for establishing the transcriptionally silent heterochromatic state. However, it is not clear
whether this low level of expression is required only to initiate the
heterochromatic state, which can be further propagated by epigenetic mechanisms such as histone methylation, or whether it is also
required for its maintenance.
The siRNAs cognate to satellite DNAs are also involved in the
epigenetic process of chromatin modification in D. melanogaster as
well as in vertebrate cells (Pal-Bhadra et al, 2004; Fukagawa et al,
2004). In D. melanogaster, their expression is developmentally regulated and is most intense in testes and in early embryos. This is probably related to the marked changes in heterochromatin that occur
during these stages (Aravin et al, 2003).
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Satellite DNA-derived siRNAs may be involved in post-transcriptional gene regulation through the action of the RNA-induced
silencing complex (RISC). This complex contains the Argonaute
protein that binds siRNA and mediates complementary mRNA
recognition and inactivation (Fig 1; Hammond et al, 2001). The
presence of several coding mRNAs in human and chick embryos
that contain α-like satellite repeats as part of their 5’ or 3’ untranslated regions indicates that their expression could be controlled by
siRNAs derived from α-satellite repeats (Li & Kirby, 2003). This is in
accordance with a model proposed by Davidson & Britten (1979)
for the coordinated expression of repeat sequences and structural
genes that contain repeat-complementary regions. It is possible that
siRNAs originating from satellite repeats have a more extensive role
in gene expression and affect both heterochromatin formation on
tandemly repeated noncoding regions and the expression of particular genes with embedded satellite repeats (Fig 1).
Conclusions
Evidence is accumulating on the functional significance of satellite
DNA sequences, in particular the uneven distribution of mutations
in satellite repeats that results in conserved and variable segments
and the extreme sequence conservation and evolutionary preservation of some satellites. Widespread transcriptional activity together
with the presence of active promoters and binding sites for different
transcription factors found in some satellite repeats further support
the functional importance of these diverse sequences. The role of
most transcripts is not known, but some are important for epigenetic
chromatin modifications and might control the expression of satellite repeat-tagged genes. Others show ribozyme activity, whereas
human satellite III transcripts are involved in the recruitment of splicing factors during stress. These examples suggest an active role for
satellite transcripts in several regulatory layers from chromatin modulation, transcription and RNA maturation to translation. As the transcription of most satellites is either developmentally and temporally
regulated or restricted to particular tissues and organs, it is plausible
that the transcripts are responsible for fine-tuning gene expression.
However, the precise biochemical mechanisms of action for different satellites and their transcripts still need to be determined.
ACKNOWLEDGEMENTS
I am grateful to M. Sopta for critical reading of the manuscript. I apologize to
those whose work could not be cited owing to space restrictions. This work was
supported by grant 0098074 from the Croatian Ministry of Science.
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EMBO reports
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